Mammalian telomere binding proteins, including Trf2 and Rap1, are essential for maintenance of telomere function and prevent the activation of aberrant DNA repair at dysfunctional telomeres. We have shown previously that disruption of Rap1 binding to Trf2 leads to rapid telomere attrition and end-to-end chromosome fusions due to homology directed repair (HDR), suggesting that Rap1 functions to repress HDR at telomeres. In addition, the N-terminal basic (B) GAR domain of TRF2 has also been shown to protect telomeres from initiating HDR. We therefore postulate that both Rap1 and Trf2 cooperate to repress telomere HDR, and that HDR-mediated repair will be exacerbated when endogenous Trf2 is replaced by a Trf2ΔB allele that is unable to interact with Rap1. We present evidence that while Rap1 cooperates with full lengthTrf2 to repress rapid telomere attrition due to HDR, it is largely dispensable for the inhibition of NHEJ-mediated fusions at uncapped telomeres.